Ever Since Owen: Changing Perspectives on the Early Evolution of

Transcription

ANRV360-ES39-27
ARI
21:3
V I E W
A
Review in Advance first posted online
on September 10, 2008. (Minor changes may
still occur before final publication
online and in print.)
N
I N
C E
S
R
E
Annu. Rev. Ecol. Evol. Syst. 2008.39. Downloaded from arjournals.annualreviews.org
by UNIVERSITY OF CHICAGO LIBRARIES on 10/21/08. For personal use only.
29 August 2008
D V A
Ever Since Owen: Changing
Perspectives on the Early
Evolution of Tetrapods
Michael I. Coates,1,2 Marcello Ruta,3
and Matt Friedman2
1
Department of Organismal Biology and Anatomy, and 2 Committee on Evolutionary Biology,
University of Chicago, Chicago, Illinois 60637; email: [email protected]
3
Department of Earth Sciences, University of Bristol, Wills Memorial Building, Queen’s Road,
Bristol BS8 1RJ, United Kingdom
Annu. Rev. Ecol. Evol. Syst. 2008. 39:571–92
Key Words
The Annual Review of Ecology, Evolution, and
Systematics is online at ecolsys.annualreviews.org
phyologeny, development, paleontology, vertebrates, limbs
This article’s doi:
10.1146/annurev.ecolsys.38.091206.095546
Abstract
c 2008 by Annual Reviews.
Copyright All rights reserved
1543-592X/08/1201-0571$20.00
The traditional notion of a gap between fishes and amphibians has been
closed by a wealth of fish-like fossil tetrapods, many discovered since the
mid 1980s. This review summarizes these discoveries and explores their
significance relative to changing ideas about early tetrapod phylogeny, biogeography, and ecology. Research emphasis can now shift to broader-based
questions, including the whole of the early tetrapod radiation, from the
divergence from other lobed-finned fishes to the origins of modern amphibians and amniotes. The fish-to-tetrapod morphological transition occurred
within the Upper Devonian; the divergence of modern tetrapod groups is an
Early Carboniferous event. Modern tetrapods emerged in the aftermath of
one of the five major extinction episodes in the fossil record, but the earlier
Devonian tetrapod radiation is not well understood. Tetrapod limbs, paired
fins, and comparative developmental data are reviewed; again, research emphasis needs to change to explore the origins of tetrapod diversity.
571
ANRV360-ES39-27
ARI
29 August 2008
21:3
INTRODUCTION
Archegosaurus (Goldfuss 1847) was the original missing link. Seized by evolutionists after Richard
Owen (1859, in Desmond 1982) declared that this “old Carboniferous reptile” conducted the
march of development from fish to primitive amphibian, the treatment of Archegosaurus foreshadowed portrayals of Ichthyostega, Acanthostega, Tiktaalik, and others besides: each depicted at pondor swamp-side with tail trailing (significantly) in the water (Milner et al. 1986). Evolutionary trees
of tetrapod ancestry have long since branched and filled to accommodate earlier and more thoroughly transitional forms (Clack 2002), but the vignette of beached missing links has persisted.
Unfortunately, this paleo-cliché reduces the exploration of tetrapod origins to the discovery of
substitute candidates for this brief episode in vertebrate history. However, questions about the origin of tetrapods now concern a much wider range of paleobiological issues. The origin of tetrapods
includes the whole of the tetrapod stem (see sidebar, Defining Tetrapod), with many groups of
fish-like (i.e., finned) taxa only recently being incorporated into this wider framework (Ahlberg &
Johanson 1998, Coates et al. 2002, Jeffery 2002, Johanson et al. 2003). It is now possible to ask
how the origins of the tetrapod total and crown groups relate to morphological changes and the
emergence of a conventional tetrapod body plan. The fin-to-limb transition is an exceptionally
rich area of integrative research and debate (e.g., Zákány et al. 1997, Coates et al. 2002, Davis
et al. 2004a,b, Friedman et al. 2007). The origin of tetrapods and the water-to-land transition are
not synonymous, but both events are associated with global climatic, atmospheric, and tectonic
changes, as well as with serial extinctions at the end of the Devonian (Algeo et al. 2001, Berner
et al. 2007, Blieck et al. 2007, Clack 2007). Taxon and character sets are now large enough to
be mined for large-scale evolutionary trends (Ruta et al. 2006, Wagner et al. 2006). This review
gathers reports and articles on this topic published in the past few years—some of which have
gained exceptionally widespread attention—and places them in context and suggests agendas for
future research.
THE POSITION OF TETRAPODS WITHIN VERTEBRATE PHYLOGENY
The first question about tetrapod origin concerns the identity of the closest relatives of land
vertebrates. This issue emerged within the nineteenth century (Desmond 1982) as discoveries
of lungfishes confounded diagnoses of living tetrapods as a natural group, and after fossil ‘rhipidistian’ fishes were recognized as belonging within the same group as limb-bearing tetrapods.
Widespread acceptance of evolutionary theory redirected systematic research to discover the particular rhipidistian ancestors of tetrapods By the early twentieth century, phylogenetic hypotheses
DEFINING A TETRAPOD
Questions associated with tetrapod origins depend on how a tetrapod is defined. Essentialist, character-based
definitions create problems because much of the research program concerning tetrapod origins aims to provide
a sequence of intermediates showing the assembly of the anatomical characters in question. Moreover, there is a
built-in presupposition that any defining character has evolved only once. In this review, we adopt phylogenetic
definitions of groups. Total-group tetrapods include all those taxa more closely related to living tetrapods than to
their nearest living sister group (lungfishes), whereas crown-group tetrapods consist of the last common ancestor
of all living tetrapods plus all the fossil and living descendants of that ancestor. Stem-group tetrapods form a
paraphyletic assemblage equivalent to the total group minus the crown group.
572
Coates
· ·
Ruta
Friedman
ANRV360-ES39-27
ARI
29 August 2008
21:3
had multiplied considerably, and ranged from polyphyletic origins of limbed vertebrates from
several ‘rhipidistian’ groups ( Jarvik 1980; Save-Soderbergh 1932, and references therein) to a
monophyletic origin from ‘osteolepiforms’ (Watson 1920; also reviewed by Panchen & Smithson
1987). Rare objections to this ‘rhipidistian’ hegemony (e.g., Kesteven 1950) were sidelined. With
tetrapod ancestry anchored to specific fossils, such as the ‘osteolepiform’ Eusthenopteron, research
focused on the adaptive circumstances surrounding the invasion of dry land.
However, by the late 1970s, this passive acceptance of ‘osteolepiforms’ as the closest fish relatives of terrestrial vertebrates provoked a reexamination of the status quo. A withering critique
of research on tetrapod origins (Rosen et al. 1981) concluded that most characters claimed to
link Eusthenopteron to tetrapods were either primitive or spurious. Emphasis was placed on the
choana, a palatal nostril framed by a diagnostic bone arrangement, present in Eusthenopteron and
tetrapods. Lungfishes also possess a palatal nostril, homologized by several nineteenth-century
anatomists with the tetrapod choana (Desmond 1982), but dismissed by most twentieth-century
paleontologists as convergent. However, newly prepared material of a Late Devonian lungfish
(Griphognathus) revealed a bone-surrounded palatal nostril that Rosen et al. (1981) offered as
evidence that a true choana was, in fact, present in primitive lungfish.
The ensuing controversy spurred paleontologists to frame explicitly cladistic hypotheses to
refute the arguments of Rosen et al. (1981) and reinstate ‘osteolepiforms’ as the closest relatives of
limbed tetrapods (e.g., Panchen & Smithson 1987, Schultze 1991). Further evidence emerged from
the discovery of the Early Devonian Diabolepis (Chang 1995, and references therein), combining
lungfish specializations with generalized sarcopterygian conditions, including possession of two
external nostrils. As the sister group of lungfishes (Chang 1995), Diabolepis indicates that lungfish
palatal nostrils are convergent with the choanae of limbed vertebrates and osteolepiforms. Two
decades later, another Chinese Devonian fish, the primitive osteolepiform Kenichthys, added a
postscript to the choana debate: its posterior nostril penetrates the skull exterior close to the
upper jaw rim, presenting a possible incipient condition for the choana (Zhu & Ahlberg 2004). A
summary of the present consensus on sarcopterygian interrelationships is shown in Figure 1 (for
further discussion see Friedman 2007).
DEVONIAN TETRAPOD DIVERSITY
Four major Devonian groups belong to the tetrapod stem lineage: rhizodonts, osteolepidids, tristichopterids, and elpistostegalids plus limbed tetrapods (Figures 1 and 2a). Most stem tetrapods
are ‘osteolepiforms’, a grade of fin-bearing groups including rhizodonts, ‘osteolepidids’, and tristichopterids, but excluding ‘elpistostegalids’. Devonian examples are known from every continent
and their diversity totals approximately 40 genera. Devonian tetrapods for which limbs have been
discovered or implied total approximately a dozen genera, although digit-bearing limbs are known
in only three: Acanthostega, Ichthyostega, and Tulerpeton. Approximately seven more unnamed forms
are reported from fragments (Clack 2005). ‘Elpistostegalids’ are the most informative taxa for understanding anatomical changes associated with the fish-to-tetrapod transition. They are known
from a handful of genera, all exclusive to the Northern Hemisphere (Daeschler et al. 2006).
Reliance upon Eusthenopteron in studies of tetrapod origins gives the false impression that
few fin-bearing tetrapods are known. In fact, many are described in detail (e.g., Fox et al. 1995;
Lebedev 1995; Long et al. 1997, 2006), but uncertainty about ‘osteolepiform’ interrelationships
obstructs deeper understanding of tetrapod origins. Rhizodonts and tristichopterids are widely
recognized as clades (Ahlberg & Johanson 1998), but few cladistic analyses have examined this
area of tetrapod phylogeny ( Johanson & Ahlberg 2001, Zhu & Ahlberg 2004). These cladograms
place Kenichthys, from the Eifelian of China, at the base of the tetrapod stem group, followed by
www.annualreviews.org • Ever Since Owen
573
ANRV360-ES39-27
ARI
29 August 2008
M
L
21:3
EG
J
EK
Permian
Triassic
Cis
Gd Lo L M
Carboniferous
Penn
Miss
Devonian
U
M
228
245
251
260
271
299
318
359
385
398
416
Ma
Total-group Actinistia
Total-group Dipnoi
Kenichthys
Osteolepis
Megalichthyidae
'Osteolepiformes'
Rhizodontida
Gogonasus
Tetrapod stem
Gyroptychius
Lissamphibian
total group
Tristichopteridae
Amniote
total group
Panderichthys
Outgroup lobefinned fish clades
Elpistostege
Tiktaalik
Elginerpeton
Limb-bearing tetrapods
Ventastega
Acanthostega
Ichthyostega
Tulerpeton
Colosteidae
Crassigyrinus
Whatcheeriidae
Baphetidae
Crown-group Lissamphibia
Temnospondyli
Embolomeri
Gephyrostegidae
Seymouriamorpha
Diadectomorpha
Tetrapod crown node
Crown-group Amniota
'Microsauria'
Lysorophia
Adelospondyli
Nectridea
Aistopoda
574
Coates
· ·
Ruta
Friedman
ANRV360-ES39-27
ARI
29 August 2008
21:3
a
b
Devonian tetrapods
1
Carboniferous tetrapods
3
2
1
4
6
5
4
7
8
2
9
3
5
6
10
7
11
9
14
12
8
11
10
13
12
15
16
13
14
15
1m
Figure 2
(a) Devonian tetrapods drawn to scale, illustrating anatomical diversity; all taxa are stem members. 1. Gooloogongia, a rhizodont;
2. Osteolepis, an ‘osteolepidid’; 3. Koharalepis, an ‘osteolepidid’; 4. Canowindra, an ‘osteolepidid’; 5. Eusthenopteron, a tristichopterid;
6. Tristichopterus, a tristichopterid; 7. Gyroptychius agassizi, an ‘osteolepidid’; 8. Gyroptychius dolichotatus, an ‘osteolepidid’; 9. Cabonnichthys,
a tristichopterid; 10. Mandageria, a tristichopterid; 11. Eusthenodon, a tristichopterid; 12. Glyptopomus, an ‘osteolepidid’; 13. Tiktaalik, an
elpistostegalid; 14. Panderichthys, an ‘elpistostegalid’; 15. Ichthyostega, a limbed stem tetrapod; 16. Acanthostega, a limbed stem tetrapod.
(b) Carboniferous tetrapods drawn to scale, illustrating anatomical diversity. Taxa shown include stem (1–5, 9, 11) and crown group
(6–8, 10, 12–15) members. 1. Strepsodus, a rhizodont; 2. Megalichthys, a megalichthyid; 3. Rhizodopsis, a megalichthyid; 4. Megalocephalus,
a baphetid (stem tetrapod); 5. Crassigyrinus, a stem tetrapod; 6. Palaeomolgophis, an adelospondyl (stem amniote or stem tetrapod);
7. Brachydectes, a lysorophid (stem amniote); 8. Urocordylus, a nectridean (stem amniote); 9. Greererpeton, a colosteid (stem tetrapod);
10. Proterogyrinus, an embolomere (stem amniote); 11. Pederpes, a whatcheeriid (stem tetrapod); 12. Westlothiana, a stem amniote;
13. Silvanerpeton, an embolomere (stem amniote); 14. Dendrerpeton, a temnospondyl (stem lissamphibian); 15. Gephyrostegus, a
gephyrostegid (stem amniote).
(in increasing proximity to the crown) rhizodonts, a paraphyletic assemblage of ‘osteolepidids’,
tristichopterids, and the clade uniting ‘elpistostegalids’ and limbed tetrapods. One solution places
the ‘osteolepidid’ Gogonasus crownward of Eusthenopteron (Long et al. 2006), but this topology
emerges from a limited taxon set (Friedman et al. 2007).
The specialized rhizodonts (2a: 1; Figure 2b: 1) branch furthest from the tetrapod crown
node. Rhizodont pectoral fins (Figure 3, top and middle) are characteristic, and have featured in
debates about tetrapod limb origin (Davis et al. 2004a), although many limb-related similarities
are probably homoplastic (Coates et al. 2002, Friedman et al. 2007). Few Devonian rhizodonts are
known: Aztecia, Gooloogongia, Sauripterus ( Johanson & Ahlberg 2001). The Frasnian Gooloogongia
←−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−
Figure 1
Evolutionary tree of early tetrapods, showing total group with taxon ranges, stem and crown taxa, and the distribution of limb-bearing
(quadrupedal) clades. Important fossil localities are listed above the geological column (M: Miguasha, Quebec, Canada; EG: East
Greenland; EK: East Kirkton, Scotland; J: Joggins, Nova Scotia, Canada). The interrelationships of finned tetrapods are adapted from
Ahlberg & Johanson (1998), whereas those of limbed tetrapods are adapted from Ruta et al. (2003).
575
ANRV360-ES39-27
ARI
29 August 2008
21:3
Eusthenopteron
('osteolepiform')
Braincase
Hyoid arch
Gill arches
Vertebral
column
Panderichthys
('elpistostegalid')
Primary
(endoskeletal)
pectoral
girdle
Primary
(endoskeletal)
pectoral fin/
forelimb
Finweb
(dermal
skeletal)
Acanthostega
(limb-bearing tetrapod)
Figure 3
Eusthenopteron (top), Panderichthys (middle), and Acanthostega (bottom), shown in lateral aspect. Anatomical
systems are color-coded. Light-shaded components of visceral skeleton in Panderichthys are inferential.
( Johanson & Ahlberg 2001) is probably the most plesiomorphic rhizodont known, but it already
exhibits most of the clade-specific specializations. Carboniferous rhizodonts achieved colossal
sizes; at an estimated length of seven meters ( Jeffery 2002), Rhizodus was probably the largest
Paleozoic osteichthyan.
‘Osteolepidids’ (: 2–4, 7, 8, 12; Figure 2b: 2, 3) lie crownward of rhizodonts and include many
generalized stem-group tetrapods. They are probably paraphyletic and their interrelationships
remain uncertain. Megalichthyids probably constitute a legitimate clade within ‘osteolepidids’.
Persisting in continental settings into the Permian, megalichthyids ( ) were the last fin-bearing
stem tetrapods.
The superficially pike-like tristichopterids are placed crownward of osteolepidids (Figure 2a:
5, 6, 9, 11). Eusthenopteron is the best-known genus, a modestly sized (80 cm) representative that
features repeatedly in debates about tetrapod origins. Tristichopterids range from the Givetian to
the Famennian, and trend toward increasing body size. The phylogenetically most basal and earliest
576
Coates
· ·
Ruta
Friedman
ANRV360-ES39-27
ARI
29 August 2008
21:3
form, Tristichopterus, was approximately 30 cm long, whereas apical members of this clade exceeded
several meters in length (Figure 2a: 10, 11; Ahlberg & Johanson 1997). Like rhizodonts, derived
tristichopterids display elongated bodies and reduced median fins (Figure 2a: 10), suggesting
convergence upon similar ecological roles (Ahlberg & Johanson 1998).
Elpistostegalids (Figure 2a: 13, 14) are the closest fish-like relatives of limbed tetrapods and
form another paraphyletic grade. Synapomorphies with limb-bearing tetrapods include a flattened
skull with dorsal orbits, a sutured dermal intracranial joint, paired frontal bones, an enlarged endoskeletal shoulder girdle, and absence of dorsal and anal fins (Ahlberg et al. 1996, Daeschler
et al. 2006, Vorobyeva & Schultze 1991). Three elpistostegalids are known in detail: Panderichthys,
Elpistostege, and Tiktaalik. Two others, Livoniana and Parapanderichthys, are known only from fragments (Ahlberg et al. 2000). The Frasnian Tiktaalik and Elpistostege appear more closely related to
limbed tetrapods than the Givetian Panderichthys (Daeschler et al. 2006). Notably, Elpistostege was
presented as a limb-bearing tetrapod (Westoll 1938) long before detailed accounts of Panderichthys
were published.
Resurgent research into tetrapod origins over the past two decades has been most apparent in
the field of limb-bearing Devonian forms ( ). When Rosen et al. (1981) appeared on the scene,
Ichthyostega (Säve-Söderbergh 1932) was the only Devonian tetrapod known to have limbs. A
detailed redescription of this taxon took over 60 years to appear ( Jarvik 1952, 1980, 1996). Acanthostega was known only from two incomplete skulls ( Jarvik 1952), whereas Metaxygnathus, an
eroded jaw from Australia, was claimed to belong to a limb-bearing tetrapod (Campbell & Bell
1977). Tulerpeton was the first Devonian newcomer to emerge, reported on the basis of an articulated trunk bearing hind- and forelimbs, the latter of which bore six digits (Lebedev & Coates
1995). It remains on the fringes of the tetrapod origins debate because its advanced characteristics
resemble post-Devonian forms.
The revolution in understanding the morphological transformation from fin-bearing to limbbearing tetrapods began with renewed expeditions to East Greenland that recovered complete
specimens of Acanthostega (Clack 2002). This material revealed an animal less than a meter in
length with a series of characters betraying its aquatic habit: a well-developed gill skeleton [Coates
& Clack 1991; a gill skeleton has subsequently been reported in Ichthyostega (Clack et al. 2003)],
paddle-like limbs bearing eight digits each (Coates 1996), and a tail with fin rays and radials (Coates
1996). These finds challenged the established notion that limbs evolved for terrestrial locomotion,
and instead placed their origin squarely within an aquatic environment.
Acanthostega also yielded a series of jaw characters unique to limbed tetrapods. The resultant
rash of new taxa based on isolated mandibles and mandible fragments has expanded the nominal diversity of Devonian forms and provided useful stratigraphic and geographic markers [Elginerpeton
(Ahlberg 1991); Ventastega (Ahlberg et al. 1994); Obruchevichthys, Densignathus (Clack 2002); Sinostega (Zhu et al. 2002); unnamed Belgian ‘ichthyostegid’ (Clement et al. 2004)]. However, although
these fragmentary taxa are conventionally described as tetrapods (in the sense of limb-bearing vertebrates rather than the total-group definition applied here), digit-bearing limbs have not been
recovered for any of them. Ventastega (Ahlberg et al. 1994, 2008) and Elginerpeton (Ahlberg 1991,
1998) each have a suite of attributed nonmandibular material. However, uncertainty surrounds the
identity of some of the Elginerpeton material, most notably the putative humerus (Ahlberg 2004,
Coates et al. 2004).
CARBONIFEROUS TETRAPOD DIVERSITY
Irrespective of finned or limbed conditions, tetrapod diversity in the earliest part of the Early
Carboniferous is poor (Figure 1); it is unclear whether this reflects impoverished faunas or simply
577
ARI
29 August 2008
21:3
a lack of available facies. This period, often referred to as Romer’s gap, occupies much of the
Tournaisian, about 360 to 350 mya. Limbed tetrapods from the upper part of the Tournaisian (about
350 to 345 mya) are known only from the nearly complete skeleton of a whatcheeriid, Pederpes,
from Scotland (Clack & Finney 2005), and fragments, mostly postcranial, from the slightly older
locality at Horton Bluff, Nova Scotia (Clack 2002). Pederpes approached a meter in length (: 11),
and, like other whatcheeriids, had a robust skull and a well-ossified postcranial skeleton with stout
limbs bearing at least five digits, probably the earliest examples suited for terrestrial walking (Clack
& Finney 2005). Further remains of similarly sized and larger whatcheeriids include Ossinodus from
the mid-Viséan of Australia (Warren 2007) and Whatcheeria from a cache of spectacularly wellpreserved skeletons from the upper Viséan of Iowa, United States (Bolt & Lombard 2000).
Unlike the limited record of Tournaisian tetrapods, the diversity of Viséan tetrapods is spectacular and Scottish sites deliver remarkable evidence of the diversification of crownward taxa. From
Gilmerton (mid-Viséan) comes the holotype of the large (nearly two meters in length), grotesque,
and Moray eel-like stem tetrapod, Crassigyrinus (Clack 2001) (: 5). The deep-sided skull resembles those of watcheeriids, but the axial skeleton is meager and the appendicular skeleton highly
reduced. Gilmerton has delivered two further large tetrapods, a baphetid and a colosteid (Clack
2002). Both examples are the earliest occurrences of their respective clades. Baphetid skulls are
large (250 mm+ in length) and many are superficially crocodile-like (: 4), although with anteriorly
extended orbits; their postcranial anatomy is mostly unknown. Colosteids are one of the more
widely represented and well-preserved groups of early, limb-bearing stem tetrapods. More than a
meter in length and with flattened skulls and postcrania, colosteids (Figure 2b: 9) resemble longtrunked giant salamanders (Godfrey 1989) and, correspondingly, are interpreted as mostly aquatic.
Unlike these bulky Gilmerton tetrapods, from Cheese Bay (also mid-Viséan) originates the
gracile, small (hip to shoulder length: 80 mm) but headless specimen of Casineria (Paton et al.
1999). This extraordinary fossil echoes the signal from Tulerpeton, displaying postcranial skeletal
anatomy far advanced beyond those of its known contemporaries, and in this instance exhibiting
characteristics of taxa close to the amniote crown.
Lethiscus (Anderson et al. 2003) from the mid-Viséan Wardie Shales of Scotland reveals a further
new aspect of tetrapod diversity: secondary limb-loss. Lethiscus is the earliest of the aı̈stopods:
snake-like with 80+ vertebrae; no trace of limbs and girdles; and, like Casineria, of small size (skull
length: 60 mm).
Adelospondyls (Andrews & Carroll 1991) represent a further clade of small (total length: 300
mm), secondarily limbless tetrapods (Figure 2b: 6) that, unlike aı̈stopods, retained their pectoral
girdle and were probably largely aquatic. Known from several sites of similar age to Cheese Bay
and Gilmerton and extending through to the Serpukhovian, adelospondyls are among the most
abundant tetrapods in the early to mid-Carboniferous beds of Scotland (Milner et al. 1986).
Aı̈stopods and adelospondyls are two subgroups of a much larger grade or clade, the lepospondyls. Often compared with small lizards and snakes, lepospondyls are characterized by possession of spool-shaped centra. Miniaturization probably underlies many of the apparent specializations manifest in this group. Other lepospondyl clades include the microsaurs, nectrideans
(: 8), lysorophids (Figure 2b: 7), and acherontiscids. The challenge of summarizing lepospondyls
within the confines of a short article underscores their remarkable morphological diversity
(Anderson 2001, Clack 2002, Ruta et al. 2003). Temporal ranges of all member clades are confined
to the Carboniferous and Permian (Milner 1993) (Figure 1).
Temnospondyls constitute a second, temporally long-ranging tetrapod group that appear first
within the Early Carboniferous. But, unlike lepospondyls, temnospondyls persist well into the
Mesozoic (Milner 1993). Temnospondyl adult size ranges vary from a few centimeters to an
estimated seven meters or more. Approximately salamander-like (although evolving into a vast
ANRV360-ES39-27
578
Coates
· ·
Ruta
Friedman
ANRV360-ES39-27
ARI
29 August 2008
21:3
range of body shapes and sizes, presumably with attendant variation in life habits), temnospondyls
exhibit usually broad and flat skulls with wide openings in the palate; the axial skeleton bears short
ribs (except in large forms) and forelimbs have four digits (: 14). Temnospondyls have long been
associated with amphibian ancestry and include the already mentioned Archegosaurus (Clack 2002,
Milner 1993).
Anthracosaurs are a third group commonly encountered in descriptions of early tetrapod diversity; once again, these have uncertain monophyletic status. Anthracosaurs also appear first in
the Early Carboniferous. They radiate throughout the remainder of the Paleozoic, and range from
small- and medium-sized terrestrial forms (: 10, 13) to large predatory aquatic genera (embolomeres, another group compared to modern crocodiles) that infested Late Carboniferous coal swamps
(Clack 2002, Holmes 1984). Putative anthracosaur synapomorphies have frequently emerged as
no more than persistent symplesiomorphies. Although long associated with the amniote stem, this
link appears to be increasingly tenuous.
The late Viséan locality of East Kirkton, Scotland, is probably the most renowned site for
Early Carboniferous tetrapods. This fossil biota is diverse (Clarkson et al. 1994) and opens a
unique window on the earliest known terrestrial vertebrate community (Ruta & Clack 2006). East
Kirkton tetrapods include a baphetid (Clack 2001), anthracosaurs (Clack 1994, Ruta & Clack
2006, Smithson 1994), and the superficially lizard-like Westlothiana (Smithson et al. 1994) (: 12).
East Kirkton lepospondyls include an undescribed microsaur ( J. Clack, work in progress) and an
aı̈stopod (Milner 1994). Temnospondyls are present, including small and large examples (Milner &
Sequeira 1994). It is noteworthy that, like Lethiscus and Casineria, these early terrestrial tetrapods
are generally small (approximately 300 mm in total length).
Many tetrapod sites are known throughout the remainder of the Carboniferous. Significant examples include Greer in West Virginia (mid-Carboniferous) and the numerous classic faunas from
coal swamps and deltaic fans of the Pennsylvanian of Illinois (Mazon Creek), Ohio (Linton), Nova
Scotia ( Joggins), Ireland ( Jarrow), England (Trawden, Newsham), and Slovakia (Nyrany) (Clack
2002, Milner et al. 1986). Unlike East Kirkton, all of these faunas have a distinctly semiaquatic
signature. The Joggins locality deserves particular mention because of its historical and biotic
significance. Dating from the mid-Bashkirian (Ryan et al. 1991), the Joggins fauna includes one of
the most primitive known temnospondyls, Dendrerpeton, as well as the earliest widely agreed-on
crown group amniote, Hylonomus (Clack 2002), a marker used repeatedly in molecular estimates
of vertebrate evolutionary history.
TREE SHAPES, NODE DATES, AND THE ORIGIN
OF CROWN-GROUP TETRAPODS
Phylogenies of early limbed tetrapods obtained from analyses of large taxon and character sets
first appeared in the mid-1990s (Carroll 1995, Laurin & Reisz 1997). Subsequent analyses (e.g.,
Laurin & Reisz 1999, Vallin & Laurin 2004) have indicated that the majority of Carboniferous
tetrapods are members of the stem group. In these trees, the earliest crown-group tetrapods are
the morphologically diverse lepospondyls, and these branch from the amphibian stem. In contrast,
the amniote stem is represented solely by diadectomorphs: bulky, stout-limbed tetrapods that first
appear in the Moscovian. More recent analyses have presented a somewhat different phylogenetic
structure (Ruta & Coates 2007, Ruta et al. 2003) in which most Carboniferous limbed tetrapods
are included within the crown. The amphibian stem is populated by temnospondyls, whereas the
lepospondyls branch from the amniote stem, along with the anthracosaurs (as shown in Figure 1).
This branching pattern conforms more closely to previous ideas about the affinities of early
tetrapods to amphibian and amniote lineages (cf. Milner et al. 1986).
579
ARI
29 August 2008
21:3
Importantly, under either phylogenetic regime, the aı̈stopod lepospondyl Lethiscus is the earliest crown-group tetrapod, dating the amphibian-amniote divergence to a minimum of around
335 mya. The equivalent fossil marker for the divergence of lungfishes and tetrapods (Diabolepis)
lies close the base of the Devonian, suggesting that the temporal span of the tetrapod stem group
exceeds 50 million years (but note that this time range lacks hard boundaries).
It is also significant that both sets of phylogenies exclude all known Devonian limbed tetrapods
from the tetrapod crown; post-Devonian limbed tetrapods are monophyletic relative to earlier
members of the clade. Acanthostega, Ichthyostega, ‘elpistostegalids’, and fragments of putative nearrelatives have not yet turned up in post-Devonian deposits. The suggestion that Tulerpeton might
represent a basal reptiliomorph (stem amniote) (Lebedev & Coates 1995) has not survived subsequent analyses (Ruta & Coates 2007, Vallin & Laurin 2004). However, an isolated humerus
from the early Carboniferous of Horton Bluff seems to link the humeri of Tulerpeton and early
anthracosaurs (Ruta & Clack 2006), whereas another study (Ruta & Bolt 2006) groups Tulerpeton
with Carboniferous whatcheeriids.
Irrespective of these tenuous connections across the Devono-Carboniferous boundary, the
topology of tetrapod phylogeny shows post-Devonian limbed tetrapods as products of a phylogenetic bottleneck (sensu Jablonski 2002), yielding a second radiation into semiaquatic ecospace.
Subsequently, by the mid-Viséan, groups of limbed tetrapods had established divergent character
complexes and, by extension, different life habits. These and many other distinguishing features
persist, in certain respects remarkably unchanged, into the later evolutionary history of the amphibian and amniote stem groups.
Evolutionary radiations are often marked by rapid diversification of new morphotypes
(Wagner 2001), and tetrapods provide an increasingly well-defined example in which the origin
of a new body-plan is associated with invasion of new habitat, as well as origin of a crown-group
radiation. Given this context, the pattern of tetrapod phylogeny might allow for comparison between contrasting models for reducing rates of morphological change (Valentine 1980): either
intrinsic constraint (i.e., developmental or genetic) or ecological restriction (i.e., filling of general ecospace). In fact, limbed tetrapods display a dramatic decrease in amounts of evolutionary
change between the Devonian and the Early Carboniferous (Ruta et al. 2006). The initial peak
of morphological evolution could easily represent relaxation of both kinds of constraint: reduced
ecological restrictions and reduced intrinsic developmental and/or genetic constraint. Decreased
rates of morphological evolution in the Early Carboniferous present a marked contrast, and these
are associated with an apparent repeated radiation into marginal terrestrial habitats. If ecology
alone were responsible for rates of morphological change, then Early Carboniferous rates ought
to mimic Devonian rates. It follows that the very marked drop in rate change could be a result of
increased intrinsic constraint. However, this assumes a simple model of empty or cleared ecospace,
whereas, at present, we have very limited knowledge of the Early Carboniferous ecosystems that
stem tetrapods occupied.
ANRV360-ES39-27
TRANSFORMATIONS: THE EMERGENCE OF A NEW BODY-PLAN
Most anatomical changes associated with the origin of limbed tetrapods occurred in groups encompassing the upper reaches of the tetrapod stem (Figure 1). Figure 2 illustrates large-scale
changes to body proportions and external features, such as fins and opercular flaps. Figure 3 details
the forequarters of three genera that have come to epitomize the fish-to-tetrapod morphological
transition: Eusthenopteron, Panderichthys, and Acanthostega.
Within the skull, the braincase (neurocranium)—primitively separated into anterior and posterior divisions—unites, and proportions change so that the anterior portion is much longer than the
580
Coates
· ·
Ruta
Friedman
ANRV360-ES39-27
ARI
29 August 2008
21:3
rear portion. The auditory capsules increase in size relative to the posterior division of the braincase, and the notochord is withdrawn from a tunnel beneath the braincase rear. These changes
are reflected in transformation of the overall skull morphology, including snout enlargement and
shifts in orbit position and orientation.
The gill skeleton (viscerocranium) is reduced, but ossified arches with deep grooves persist in
the earliest limbed tetrapods. The hyoid arch is transformed as the palate (not shown) becomes
attached securely to the braincase. The lower division of the hyoid arch, the ceratohyal, remains
large and probably retained primitive functions associated with jaw, gill arch, and oropharyngeal
volume change. The upper division, the hyomandibula, is reduced and reoriented as a primitive
stapes. Instead of articulating wholly with the ossified sidewall of the auditory capsule, the proximal
end of the nascent stapes sits mostly within an unossified window. No longer associated clearly with
jaw suspension, the hyomandibula/stapes might have had an incipient role in sound conduction
and/or spiracular pouch function (Clack 2002, 2007).
Postcranially, the persistently notochordal vertebral column gains expanded centra and upright
neural spines, while ribs enlarge, acquire broad heads, and extend laterally. Separation of the
pectoral girdle from the skull creates a neck allowing lateral movement of the head (relative to the
trunk). The endoskeletal scapulocoracoid is enlarged, buttressed, and reorients to face laterally.
Dermal bones of the pectoral girdle are reduced dorsally and laterally, but enlarged and expanded
ventrally. Not illustrated but of clear functional significance, the pelvis enlarges and acquires direct
attachment, by means of one or more sacral ribs, to the vertebral column. Associated with this,
the hip socket (acetabulum) and surrounding buttresses are reoriented, as in the scapulocoracoid,
to face laterally.
Finally, scale coverage of the body and fins is reduced dramatically in limbed tetrapods relative
to ‘elpistostegids’ (and other finned stem-taxa; Figure 4f ). In early limbed tetrapods, ossified
scales are present only as gastralia, scales on the ventral surface of the trunk [Ichthyostega presents
a notable exception, with reported cycloid scales on the tail ( Jarvik 1952)].
THE ORIGIN OF TETRAPOD LIMBS: MORPHOLOGICAL NOVELTY
The fin-to-limb transition concerns separate events at pectoral and pelvic levels, and there is
evidence that several changes occurred first at pelvic level (Coates et al. 2002). The following
summary focuses on forelimbs because the data set is slightly more detailed. Key events concern fin
ray loss, digit acquisition, and remodeling of the humerus. The resultant tripartite organization as
stylopod (humerus), zeugopod (radius and ulna), and autopod (wrist and digits) presumably reflects
the phylogenetic emergence of developmental autonomy within the outgrowing limb, in which
the zeugopod initially resembles a carry-over from the primitive (fin) condition (Figure 4a–g).
Figure 4 shows Devonian and Carboniferous tetrapod pectoral fin and limb endoskeletons.
Tetrapod fin skeletons (Figure 4a–g) are clearly different from limb skeletons, and, as argued by
Rosen et al. (1981), they retain an essentially primitive, asymmetrically branched pattern (Friedman
et al. 2007). Within a phylogeny of tetrapod fins and limbs, the longest internal branch (length
proportional to total character-state change) spans the fin-to-limb divide (Coates et al. 2002).
Only the Late Devonian Catskill humerus (Shubin et al. 2004) slots into this gap, and the question
of whether it supported fin rays or digits remains unanswered.
All fins shown (Figure 4a–g) supported ossified and segmented fin rays, and, in life, the endoskeleton was encased within a scale-covered muscular lobe (only shown in). Primitively, the
radius is consistently longer than the ulna. The humerus has been described as the first mesomere
or segment of an axis drawn through the ulna and ulnare toward the outermost extremity of
the fin. Usually labeled the metapterygial axis (Coates 2003, Grandel 2003), this easily maps
581
ANRV360-ES39-27
ARI
29 August 2008
21:3
a
b
c
Humerus
Radius
Ulna
d
e
h
f
i
g
j
k
Figure 4
Fin and limb skeletons. (a) Sauripterus, a rhizodont, after Davis et al. (2004a). (b) Barameda, a rhizodont, after
Long (1989) and Garvey et al. (2005). (c) Tiktaalik, an ‘elpistostegalid’, after Shubin et al. (2006).
(d ) Eusthenopteron, a tristichopterid, after Andrews & Westoll (1970). (e) Gogonasus, an ‘osteolepidid’, after
Long et al. (2006). ( f ) Sterropterygion, a megalichthyid (original). ( g) Rhizodopsis, a megalichthyid, after
Friedman et al. (2007). (h) Acanthostega, a limb-bearing stem tetrapod, after Coates (1996). (i) Tulerpeton, a
limb-bearing stem tetrapod, after Lebedev & Coates (1995). ( j) Greererpeton, a limb-bearing stem tetrapod,
after Coates (1996). (k) Westlothiana, a stem amniote, after Smithson et al. (1994). Dermal fin skeleton,
comprising fin rays and scales, are shown in light gray for Sterropterygion ( f ); similarly elaborate dermal
skeletons are present, but not illustrated, in all taxa in the top two rows. These features are absent from the
digit-bearing taxa in the bottom row. All skeletons are shown with leading edge to right of Figure; all are in
dorsal aspect except for (a) and ( f ) (ventral aspect).
582
Coates
· ·
Ruta
Friedman
ANRV360-ES39-27
ARI
29 August 2008
21:3
out to the third or fourth mesomere, but the pattern is often indistinct distally (Friedman et al.
2007). None of these skeletons is outstandingly limb-like. Although the pectoral fin of Tiktaalik
( ) is related most closely to digit-bearing limbs (Shubin et al. 2006), unambiguously limb-like
characteristics are restricted to humerus shape.
Digits can be regarded as a subgroup of radials, but they possess distinguishing characteristics,
including alignment as a series across the distal end of the appendage (functionally uniting distal
ends of the radius and ulna) and the absence of a distally branched pattern. Furthermore, digits
are known only in appendages where fin rays and scales are absent. In primitive limb skeletons
(Figure 4h–k) the humerus is L-shaped with a large, posterior flange, the entepicondyle. There is
a distinct elbow joint; distal to this the limb skeleton generally flexed (contrast Figure 4h–k with
4a–i ). Several trends are apparent from the most primitive (Acanthostega, Figure 4h) to the most
advanced (Westlothiana, Figure 4k) examples shown. The humerus gains a shaft; the ulna extends
to equal radius length; the intermedium is moved into the wrist region (instead of flanking the
radius); a complex wrist joint (including a noncylindrical intermedium) intercalates between the
radius, ulna, and digits; and digit numbers diminish to stabilize at five.
THE ORIGIN OF TETRAPOD LIMBS: DEVELOPMENTAL CHANGE
Most information about vertebrate limb development has been obtained from studies of chicks
and mice [reviewed recently by Tanaka & Tickle (2007)]. Fin data are largely from the teleost
zebrafish (Grandel 2003), although further data are being obtained from paddlefish (nonteleost
actinopterygians) (Davis et al. 2007, Metscher et al. 2005), lungfish (sarcopterygians) ( Johanson
et al. 2007), and elasmobranch chondrichthyans (Dahn et al. 2007, Freitas et al. 2007). Importantly,
it appears that bony fishes as a whole (from tetrapods to teleosts) share most of the same genes
and developmental regulatory systems, and that most of the same materials examined thus far are
deployed and used similarly in paired fin buds and limb buds.
Digit primordia appear late in limb bud development, and some of the most widely discussed
work on this aspect of limb development concerns the similarly late and distal activity of particular
Hox genes and how this might affect digit patterning. Hox gene nested expression patterns in
outgrowing limb buds are dynamic and phased (Zakany et al. 1997) and relate to proximo-distal
patterning (Wellik & Capecchi 2003, Tarchini & Duboule 2006). A subset of Hox genes is expressed
at high levels in the digit-forming region (Kmita et al. 2002), and this expression phase was thought
to be absent in paired fins. Functional studies provide important clues about the significance of
this episode in digit patterning, as well as the evolutionary assembly of this regulatory architecture
(Kmita et al. 2002, Tarchini & Duboule 2006, Zakany et al. 1997).
These data contributed to the notion of the distal region of tetrapod limbs, including digits
and the wrist/ankle (the autopod), as an evolutionary novelty (Wagner & Chiu 2001). However,
discovery of an autopodial-like Hox gene expression pattern in the developing paired fins of
osteichthyans and chondrichthyans (Davis et al. 2007, Freitas et al. 2007) suggests otherwise
(consistent with patches of Hox gene expression in lungfish fins: Johanson et al. 2007). It appears
increasingly likely that aspects of autopodial developmental patterning are general characteristics
of paired fin buds in all gnathostomes. Just as digits can be characterized as a new and precise
arrangement of fin radials, their development probably co-opted more general patterns of gene
regulatory activity (Friedman et al. 2007, Grandel 2003).
In contrast, fin rays are unambiguously unique to fins. Fin rays are components of the dermal
skeleton (rather than endoskeleton), and the dermal skeleton is a derivative of the neural crest.
Trunk crest has evident skeletogenic potential, although in living tetrapods this capacity is only
expressed by the cranial neural crest (McGonnell & Graham 2002). Fin rays develop within the
583
ARI
29 August 2008
21:3
apical fold of an embryonic fin bud (Grandel 2003, Witten & Huysseune 2007) and this fold
is an outgrowth of the apical ectodermal ridge, a major signaling center involved in limb bud
development. Loss of fin rays during the evolutionary origin of limbs implies significant change in
the developmental activity of the apical ectodermal ridge. Proximodistal patterning, outgrowth,
and anteroposterior patterning result from complex feedback-linked signal systems between the
apical ridge and other signaling centers of limb and fin buds. Moreover, experimental and clinical
studies show that large-scale morphological abnormalities occur when such signals are disrupted
(Tanaka & Tickle 2007).
These differences between fins and limbs have barely been considered from a comparative
and evolutionary standpoint (Freitas et al. 2007): the transition from apical ectodermal ridge to
apical fold, the arrest or persistence (in development) of an apical signaling center, the possible
presence and influence of skeletogenic neural crest mesenchyme. Any or all of these probably
interlinked factors, subject to natural variation, seem likely to have provided the material basis for
morphologically significant and perhaps rapid evolutionary change.
ANRV360-ES39-27
THE ORIGIN OF TETRAPOD LIMBS: FUNCTIONAL CHANGE
As in discussions of developmental change, scenarios of functional change at the fin-to-limb
transition have focused on the endoskeleton, whereas the role of scales and fin rays has been
neglected. The suggestion that limbs evolved in a primitively aquatic taxon is based on conjunction
of paddle-like limbs, grooved gill bars, and skeletally supported tail fin in Acanthostega (Coates 1996,
Clack 2002). However, this now accompanies discussions of load-bearing fins in Tiktaalik (Shubin
et al. 2006) and other stem tetrapods (Boisvert 2005). These speculations need not be mutually
exclusive, because vertebrate exploitation of marginal aquatic habitats probably happened under
different ecological circumstances for a variety of tetrapod groups, just as occurs today for many
kinds of teleost fishes (Graham 1997).
As for speculation about the biomechanics of limb-like fins, few substantial studies have been
completed. Histological analysis of the paired fin skeletons of Eusthenopteron (, top; Figure 4d )
indicates that this stem tetrapod, at least, was wholly aquatic (Laurin et al. 2007). Among the
descriptions of walking gaits in living fishes (Pridmore 1995, Wilga & Lauder 2001, Lucifora &
Vassallo 2002a) an axial-driven walking trot has been proposed as primitive for tetrapods (Pridmore
1995). However, within stem tetrapods this aquatic walking trot was probably superseded by
a pelvic-driven bipedal gait, because air-filled lungs would have supported the anterior trunk
region. Such a scenario is consistent with the phylogenetic sequence of limb evolution, in which
conventional limb characteristics occur first in pelvic appendages (Coates et al. 2002). Fossil trackway data might deliver further insights (Clack 2002), but assigning Devonian tracks to the earliest
limbed tetrapods is especially difficult, given the paddle-like form and orientation of primitive
hind limbs.
HABITATS AND PALEOBIOGEOGRAPHY
Thus far, the late Givetian to early Frasnian ‘elpistostegalids’ are confined to the fringe of Euramerica (Daeschler et al. 2006) (Figure 5). The Euramerican fringe also includes the Viséan midland
valley of Scotland, source of the earliest crown-group tetrapods. Sandwiched between these last
two groups, the earliest limbed (and less-certainly limbed) genera have been collected from a wide
area, including the Frasnian-Famennian of Euramerica, North China, and easternmost Gondwana
(Blieck et al. 2007). The paleoenvironments of these Late Devonian tetrapods range from proximal, near-shore marine localities to continental, freshwater lakes and rivers (Blieck et al. 2007,
584
Coates
· ·
Ruta
Friedman
ANRV360-ES39-27
ARI
29 August 2008
21:3
14 24
15 18 19 20 21 22
Lower
Carboniferous
359–318 Ma
16
23
17
Sites yielding
# elpistostegalian-
grade taxa
Sites yielding taxa
# known or believed
7 13
1
Middle–Upper
Devonian
387–359 Ma
3
to be limb bearing
5 11
12
4
82
10 9
Figure 5
Devonian and Carboniferous paleogeographic maps (adapted, with permission, from originals by Ron Blakey, Northern Arizona
University) marked with numbers corresponding to the following important tetrapod localities (black numerals indicate localities
yielding elpistostegalid-grade taxa, whereas red numerals denote sites yielding forms either known or believed to have been limb
bearing). Middle and Upper Devonian sites (taxon lists adapted from Clack 2007): 1, Gauja Formation, Latvia and Estonia (upper
Givetian; Livoniana, Panderichthys); 2. Miguasha, Quebec, Canada (lower Frasnian; Elpistostege); 3. Fram Formation, Nunavut, Canada
(lower Frasnian; Tiktaalik); 4. Scat Crag, Scotland (upper Frasnian, Elginerpeton); 5. Velna-Ala, Latvia (upper Frasnian; Obruchevichthys);
6. Jemalong, New South Wales, Australia (upper Frasnian-lower Famennian; Metaxygnathus); 7. Gornostayevka quarry, Russia (lower
Famennian; Jakubsonia); 8. Aina Dal and Britta Dal formations, East Greenland (upper Famennian; Acanthostega, Ichthyostega, new
genus); 9. Evieux Formation, Belgium (upper Famennian; Ichthyostega-like form); 10. Catskill Formation, Pennsylvania, USA (upper
Famennian; Catskill humerus, Densignathus, Hynerpeton, whatcheerid-like form); 11. Ketleri and Pavāri, Latvia (upper Famennian;
Ventastega); 12. Ningxia, China (upper Famennian; Sinostega); 13. Andreyevka-2, Russia (uppermost Famennian; Tulerpeton). Lower
Carboniferous sites (taxon lists adapted from Clack 2002, Milner et al. 1986): 14. Horton Bluff, Nova Scotia, Canada (Tournaisian);
15. Ballagan Formation, Scotland (middle Tournaisian; Pederpes); 16. Delta, Iowa, USA (lower Viséan; Whatcheeria); 17. Duckabrook
Formation, Queensland, Australia (lower Viséan; Ossinodus); 18. Wardie, Scotland (lower Viséan; Lethiscus); 19. East Kirkton, Scotland
(middle Viséan; see text for taxon list); 20. Cheese Bay, Scotland (middle Viséan; Casineria); 21. Gilmerton Quarry, Scotland (middle
Viséan; Crassigyrinus, Loxomma, colosteid); 22. Dora, Scotland (upper Viséan; Crassigyrinus, Doragnathus, Eoherpeton, Proterogyrinus,
adelogyrinid); 23. Greer, West Virginia, USA (upper Viséan-lower Serpukhovian; Greererpeton, Proterogyrinus). 24. The well-known
Joggins locality (Upper Carboniferous, mid-Bashkirian).
585
ANRV360-ES39-27
ARI
29 August 2008
21:3
Lebedev 2004). Paleocontinental reconstruction (Averbuch et al. 2005) indicates that all 10 noted
localities for what might be the earliest limbed tetrapods lie within 30◦ of the estimated equator,
consistent with macroevolutionary ideas about cradles of diversity (Goldberg et al. 2005). However, it remains unclear whether this distribution is the result of collection bias. Marginal deposits
of Late Devonian age have not been fully exploited in Africa, South America, or Antarctica.
THE END DEVONIAN EXTINCTION AND RECOVERY
The Late Devonian extinction, marked by an estimated loss of between 70% and 82% of marine
species (McGhee 2001), extended from the latest Frasnian and into the Famennian. This drawnout biotic crisis has been correlated with global cooling ( Joachimski & Buggisch 2002, Streel et al.
2000), atmospheric change (Berner et al. 2007, Scott & Glasspool 2006, Algeo et al. 2001), and the
radiation of terrestrial plants leading to aquatic eutrophication and anoxia on an intercontinental
scale (Algeo et al. 2001). Furthermore, the Late Devonian was a period of intense tectonic activity,
with incipient collisions of continental crustal blocks including Laurussia, Gondwana, Kazakhstan,
and Siberia (Averbuch et al. 2005). These tectonic events closed entire oceanic domains (Figure 5),
had a widespread influence on other marine environments, and probably contributed to global
cooling (Averbuch et al. 2005, Blieck et al. 2007).
Tetrapods (the total group) originated prior to this episode of massive change, and by the end of
it, most of the group seems to have perished. The greening (aquatic and terrestrial) of continents,
from the late Silurian through to the Middle Devonian, was a late phase in a vast sequence of continental invasions (Labandeira 2005). But those processes that provided the structural and trophic
complexity necessary for terrestrial vertebrate life might also have been those that devastated the
tetrapod clade (Algeo et al. 2001).
The ∼15 million year post-Devonian trough in the record of limbed tetrapods (Clack 2002,
Ruta et al. 2003) is also apparent in the fossil history of terrestrial arthropods (Ward et al. 2006).
Absence of both groups throughout most of the Tournaisian has been attributed (Ward et al.
2006) to an estimated trough in atmospheric oxygen levels (Berner et al. 2007), constraining
both groups to aquatic habitats. Physiological arguments have some bearing on this scenario,
but the sudden diversity of Viséan limbed tetrapods implies that this gap might equally reflect
unevenness of the fossil record (Clack 2007). Tetrapod phylogeny clearly underwent multiple
branching events and encompassed considerable morphological diversification during this interval,
the results of which include aı̈stopods, adelogyriniids, temnospondyls, and Westlothiana (and we
have correspondingly little idea about any hidden diversity of as yet unknown post-Devonian
‘elpistostegalids’, ‘acanthostegids’, and ‘ichthyostegids’). If there is any signature in the tetrapod
record that might be more safely attributed to early Carboniferous atmospheric conditions, then
it is the reduced size of these crown tetrapods and their close relatives (Figure 2), compared with
the larger dimensions of earlier and more basally branching clades (Clack 2007).
CONCLUSIONS AND FUTURE DIRECTIONS
Early tetrapod distribution is clumpy at any scale, from detailed features of anatomy (note the
almost bimodal array paired fin and limb skeletons; Figure 4) up to the patchy distribution of
body shapes and higher taxonomic categories. These patterns should be investigated; it seems unlikely that they result wholly from extinctions editing chunks from evenly spread morphological
continuity (cf. Erwin 2007). The use of nontraditional node-based rather than character-based
group definitions is disputed (Blieck et al. 2007, Clack 2007), but it permits a better perspective of
early tetrapod evolution, and provides an explicit means of framing questions about group origins
586
Coates
· ·
Ruta
Friedman
ANRV360-ES39-27
ARI
29 August 2008
21:3
and change. The “vast structural gaps” (Milner et al. 1986) separating Ichthyostega from ‘osteolepiforms’ and Carboniferous tetrapods have effectively closed: The research program started
by Owen approximately 150 years ago is largely completed. Narratives of morphological change
from fish to tetrapod can be refined, but there are other issues to address. The turnover in clade
composition across the Devono-Carboniferous boundary is dramatic, and we note that it yields
two groups that radiate significantly within the post-Devonian Paleozoic: limbed tetrapods and
rhizodontids. If research explores only the limbed subset of the tetrapod total group, much of the
evolutionary signal will be missed (as if research on mammal evolution ignored noneutherians).
A detailed phylogenetic analysis of the whole of the tetrapod stem is needed. Similarly, Devonian
tetrapod-containing biotas need to be subjected to the level of study applied to Carboniferous
localities such as East Kirkton (Clarkson et al. 1994). Paleoecological understanding of the earliest tetrapods would also be assisted by substantial biomechanical analyses of structures such as
lobed fins, and vertebrae retaining a large notochordal component. Finally, developmental analyses of differences between fins and limbs, rather than searches for general, and perhaps primitive,
conditions, would accelerate our understanding of present and past morphological diversity.
DISCLOSURE STATEMENT
The authors are not aware of any biases that might be perceived as affecting the objectivity of this
review.
ACKNOWLEDGMENTS
Much of what we currently understand about the early evolution of tetrapods is directly or indirectly attributable to Alec Panchen (a significant proportion of the work cited here might be
regarded as the output of his extended research group), and Stanley Wood (for discoveries of early
tetrapods and localities such as East Kirkton). Research supported by the Faculty Research Fund,
Pritzker School of Medicine, University of Chicago (MIC); Environmental Protection Agency
STAR Fellowship (award number FP 916730; MF).
LITERATURE CITED
Ahlberg PE. 1991. Tetrapod or near-tetrapod fossils from the Upper Devonian of Scotland. Nature 354:298–
301
Ahlberg PE. 1998. Postcranial stem tetrapod remains from the Devonian of Scat Craig, Morayshire, Scotland.
Zool. J. Linn. Soc. 122:99–141
Ahlberg PE. 2004. Comment on “The Early Evolution of the Tetrapod Humerus.” Science 305:1715
Ahlberg PE, Clack JA, Luksevics E. 1996. Rapid braincase evolution between Panderichthys and the earliest
tetrapods. Nature 381:61–64
Ahlberg PE, Clack JA, Luksevics E, Blom H, Zupins E. 2008. Ventastega curonica and the origin of tetrapod
morphology. Nature 453:1199–1204
Ahlberg PE, Johanson Z. 1997. Second tristichopterid (Sarcopterygii, Osteolepiformes) from the Upper Devonian of Canowindra, New South Wales, Australia, and phylogeny of the Tristichopteridae. J. Vert.
Paleontol. 17:653–73
Ahlberg PE, Johanson Z. 1998. Osteolepiforms and the ancestry of tetrapods. Nature 395:792–94
Ahlberg PE, Luksevics E, Lebedev O. 1994. The first tetrapod finds from the Devonian (Upper Famennian)
of Latvia. Philos. Trans. R. Soc. London Ser. B 343:303–28
Ahlberg PE, Luksevics E, Mark-Kurik E. 2000. A near-tetrapod from the Baltic Middle Devonian. Palaeontology
43:533–48
587
ARI
29 August 2008
21:3
Algeo TJ, Scheckler SE, Maynard JB. 2001. Effects of the Middle to Late Devonian spread of vascular land
plants on weathering regimes, marine biotas, and global climate. In Plants Invade the Land: Evolutionary
and Environmental Perspectives, ed. P Gensel, D Edwards, pp. 213–36. New York: Columbia Univ. Press
Anderson JS. 2001. The phylogenetic trunk: maximal inclusion of taxa with missing data in an analysis of the
Lepospondyli (Vertebrata, Tetrapoda). Syst. Biol. 50:170–93
Anderson JS, Carroll RL, Rowe TB. 2003. New information on Lethiscus stocki (Tetrapoda: Lepospondyli:
Aı̈stopoda) from high-resolution computed tomography and a phylogenetic analysis of Aı̈stopoda. Can.
J. Earth Sci. 40:1071–83
Andrews SM, Carroll RL. 1991. The order Adelospondyli: Carboniferous lepospondyl amphibians. Trans. R.
Soc. Edinb.: Earth Sci. 82:239–75
Andrews SM, Westoll TS. 1970. The postcranial skeleton of Eusthenopteron foordi Whiteaves. Trans. R. Soc.
Edinb. 68:207–329
Averbuch O, Tribovillard N, Devleeschouwer X, Riquier L, Mistiaen B, et al. 2005. Mountain buildingenhanced continental weathering and organic carbon burial as major causes for climatic cooling at the
Frasnian-Famennian boundary (c. 376 Ma)? Terra Nova 17:25–34
Berner RA, Vandenbrooks JM, Ward PD. 2007. Oxygen and evolution. Science 316:557–58
Blieck A, Clement G, Blom H, Lelievre H, Luksevics E, et al. 2007. The biostratigraphical and palaeogeographical framework of the earliest diversification of tetrapods (Late Devonian). Geol. Soc. London Spec.
Publ. 278:219–35
Boisvert CA. 2005. The pelvic fin and girdle of Panderichthys and the origin of tetrapod locomotion. Nature
438:1145–47
Bolt JR, Lombard RE. 2000. Palaeobiology of Whatcheeria deltae, a primitive Mississippian tetrapod. In Amphibian Biology, 4: Palaeontology, ed. H Heatwole, RL Carroll, pp. 1044–52. Chipping Norton: Surrey
Beatty & Sons
Campbell KSW, Bell MW. 1977. A primitive amphibian from the Late Devonian of New South Wales.
Alcheringa 1:369–81
Carroll RL. 1995. Problems of the phylogenetic analysis of Paleozoic choanates. Bull. Mus. Natl. Hist. Nat.,
Paris, 4e sér., Sect. C 17:389–445
Chang MM. 1995. Diabolepis and its bearing on the relationships between porolepiforms and dipnoans. Bull.
Mus. Natl. Hist. Nat., Paris 17:235–68
Clack JA. 1994. Silvanerpeton miripedes, a new anthracosauroid from the Viséan of East Kirkton, West Lothian,
Scotland. Trans. R. Soc. Edinb.: Earth Sci. 84:369–76
Clack JA. 1998. The Scottish Carboniferous tetrapod Crassigyrinus scoticus (Lydekker)—cranial anatomy and
relationships. Trans. R. Soc. Edinb.: Earth Sci. 88:127–42
Clack JA. 2001. Eucritta melanolimnetes from the Early Carboniferous of Scotland, a stem tetrapod showing a
mosaic of characteristics. Trans. R. Soc. Edinb.: Earth Sci 92:75–95
Clack JA. 2002. Gaining Ground. The Origin and Evolution of Tetrapods. Bloomington: Indiana Univ. Press.
403 pp.
Clack JA. 2005. Making headway and finding a foothold: tetrapods come ashore. In Evolving Form and Function:
Fossils and Development, ed. GDE Briggs, pp. 223–44. Peabody Mus. Nat. History Spec. Publ. New Haven,
CT: Yale Univ.
Clack JA. 2007. Devonian climate change, breathing, and the origin of the tetrapod stem group. Integr. Comp.
Biol. 47:510–23
Clack JA, Ahlberg PE, Finney SM, Dominguez Alonso P, Robinson J, et al. 2003. A uniquely specialized ear
in a very early tetrapod. Nature 425:65–69
Clack JA, Finney SM. 2005. Pederpes finneyae, an articulated tetrapod from the Tournaisian of Western Scotland.
J. Syst. Palaeontol. 2:311–46
Clarkson ENK, Milner AR, Coates MI. 1994. Palaeoecology of the Viséan of East Kirkton, West Lothian,
Clément G, Ahlberg PE, Blieck A, Blom H, Clack JA, et al. 2004. Devonian tetrapod from western Europe.
Nature 427:412–13
Coates MI. 1996. The Devonian tetrapod Acanthostega gunnari Jarvik: postcranial anatomy, basal tetrapod
interrelationships and patterns of skeletal evolution. Trans. R. Soc. Edinb.: Earth Sci. 87:363–422
ANRV360-ES39-27
588
Coates
· ·
Ruta
Friedman
ANRV360-ES39-27
ARI
29 August 2008
21:3
Coates MI. 2003. The evolution of paired fins. Theory Biosci. 122:266–87
Coates MI, Clack JA. 1991. Fish-like gills and breathing in the earliest known tetrapod. Nature 352:234–36
Coates MI, Jeffery JE, Ruta M. 2002. Fins to limbs: what the fossils say. Evol. Dev. 4:390–401
Coates MI, Shubin NH, Daeschler EB. 2004. Response to Comment on “The Early Evolution of the Tetrapod
Humerus.” Science 305:1715
Daeschler EB, Shubin NH, Jenkins FA Jr. 2006. A Devonian tetrapod-like fish and the evolution of the tetrapod
body plan. Nature 440:757–63
Dahn RD, Davis MC, Pappano WN, Shubin NH. 2007. Sonic hedgehog function in chondrichthyan fins and
the evolution of appendage patterning. Nature 445:311–14
Davis MC, Dahn MC, Shubin NH. 2007. An autopodial-like pattern of Hox expression in the fins of a basal
actinopterygian fish. Nature 447:473–76
Davis MC, Shubin NH, Daeschler EB. 2004a. A new specimen of Sauripterus taylori (Sarcopterygii, Osteichthyes) from the Famennian Catskill Formation of North America. J. Vert. Paleontol. 24:26–40
Davis MC, Shubin NH, Force A. 2004b. Pectoral fin and girdle development in the basal actinopterygians
Polyodon spathula and Acipenser transmontanus. J. Morphol. 262:608–28
Desmond AJ. 1982. Archetypes and Ancestors. Chicago: Univ. Chicago Press. 288 pp.
Erwin DH. 2007. Disparity: morphological pattern and developmental context. Palaeontology 50:57–73
Fox RC, Campbell KSW, Barwick RE, Long JA. 1995. A new osteolepiform fish from the Lower Carboniferous
Raymond Formation, Drummond Basin, Queensland. Mem. Queensl. Mus. 38:99–221
Freitas R, Zhang G, Cohn MJ. 2007. Biphasic hoxd gene expression in shark paired fins reveals an ancient
origin of the distal limb domain. PLoS ONE 8:e754
Friedman M. 2007. Styloichthys as the oldest coelacanth: implications for early osteichthyan interrelationships.
Friedman M, Coates MI, Anderson P. 2007. First discovery of a primitive coelacanth fin fills a major gap in
the evolution of lobed fins and limbs. Evol. Dev. 9:329–37
Garvey JM, Johanson Z, Warren A. 2005. Redescription of the pectoral fin and vertebral column of the
rhizodontid fish Barameda decipiens from the Lower Carboniferous of Australia. J. Vert. Paleontol. 25:8–18
Godfrey SJ. 1989. The postcranial skeletal anatomy of the Carboniferous tetrapod Greererpeton burkemorani.
Philos. Trans. R. Soc. London Ser. B 323:75–133
Goldberg EE, Roy K, Lande R, Jablonski D. 2005. Diversity, endemism, and age distributions in macroevolutionary sources and sinks. Am. Nat. 165:623–33
Goldfuss GA. 1847. Beiträge zur vorweltlichen Fauna des Steinkohlengebirges. Bonn: Nat. Ver. Preußischen Rheinl.
30 pp.
Graham JB. 1997. Air-breathing Fishes: Evolution, Diversity, and Adaptation. San Diego, CA: Academic. 320 pp.
Grandel H. 2003. Approaches to a comparison of fin and limb structure and development. Theory Biosci.
122:288–301
Holmes RB. 1984. The Carboniferous amphibian Proterogyrinus scheelei Romer, and the early evolution of
tetrapods. Philos. Trans. R. Soc. London Ser. B 306:431–527
Jablonski D. 2002. Survival without recovery after mass extinctions. Proc. Natl. Acad. Sci. USA 99:8139–44
Jarvik E. 1952. On the fish-like tail in the ichthyostegid stegocephalians with descriptions of a new stegocephalian and a new crossopterygian from the Upper Devonian of East Greenland. Medd. Grönland
114:1–90
Jarvik E. 1980. Basic Structure and Evolution of Vertebrates. Vols. 1, 2. New York: Academic. 575 pp. 337 pp.
Jarvik E. 1996. The Devonian tetrapod Ichthyostega. Foss. Strata 40:1–206
Jeffery JE. 2002. Mandibles of rhizodontids: anatomy, function and evolution within the tetrapod stem-group.
Trans. R. Soc. Edinb.: Earth Sci. 93:255–76
Joachimski MM, Buggisch W. 2002. Conodont apatite d18 O signatures indicate climatic cooling as a trigger
of the Late Devonian mass extinction. Geology 30:711–14
Johanson Z, Ahlberg PE. 2001. Devonian rhizodontids (Sarcopterygii; Tetrapodomorpha) from East
Gondwana. Trans. R. Soc. Edinb.: Earth Sci. 92:43–74
Johanson Z, Ahlberg PE, Ritchie A. 2003. The braincase and palate of the tetrapodomorph sarcopterygian
Mandageria fairfaxi: morphological variability near the fish-tetrapod transition. Palaeontology 46:271–93
589
ARI
29 August 2008
21:3
Johanson Z, Joss J, Boisvert CA, Ericsson R, Sutija M, Ahlberg PE. 2007. Fish fingers: digit homologues in
sarcopterygian fish fins. J. Exp. Zool. B 308:757–68
Kesteven HL. 1950. The origin of the tetrapods. Proc. R. Soc. Vic. 59:93–138
Kmita M, Fraudeau N, Hérault Y, Duboule D. 2002. Serial locus deletions and duplications in vivo suggest a
mechanism for HoxD genes colinearity in developing limbs. Nature 420:145–50
Labandeira CC. 2005. Invasion of the continents: cyanobacterial crusts to tree-inhabiting arthropods. Trends
Ecol. Evol. 20:253–62
Laurin M, Meunier FJ, Germain D, Lemoine M. 2007. A microanatomical and histological study of the paired
fin skeleton of the Devonian sarcopterygian Eusthenopteron foordi. J. Paleontol. 81:143–53
Laurin M, Reisz RR. 1997. A new perspective on tetrapod phylogeny. In Amniote Origins: Completing the
Transition to Land, ed. SS Sumida, KLM Martin, pp. 9–59. London: Academic
Laurin M, Reisz RR. 1999. A new study of Solenodonsaurus janenschi, and a reconsideration of amniote origins
and stegocephalian evolution. Can. J. Earth Sci. 36:1239–55
Lebedev OA. 1995. Morphology of a new osteolepidid fish from Russia. Bull. Mus. Natl. Hist. Nat., Paris, 4e
sér., Sect. C 17:287–341
Lebedev OA. 2004. A new tetrapod Jakubsonia livnensis from the Early Famennian (Devonian) of Russia and
palaeoecological remarks on the Late Devonian tetrapod habitats. Acta Univ. Latv. 679:79–98
Lebedev OA, Coates MI. 1995. The postcranial skeleton of the Devonian tetrapod Tulerpeton curtum Lebedev.
Zool. J. Linn. Soc. 114:307–48
Long JA. 1989. A new rhizodontiform fish from the Early Carboniferous of Victoria, Australia, with remarks
on the phylogenetic position of the group. J. Vert. Paleontol. 9:1–17
Long JA, Barwick RE, Campbell KSW. 1997. Osteology and functional morphology of the osteolepiform fish
Gogonasus andrewsae Long, 1985, from the Upper Devonian Gogo Formation, Western Australia. Rec.
West. Aust. Mus. 53:1–89
Long JA, Young GC, Holland T, Senden TJ, Fitzgerald EMG. 2006. An exceptional Devonian fish from
Australia sheds light on tetrapod origins. Nature 444:199–202
Lucifora LO, Vassallo AI. 2002. Walking in skates (Chondrichthyes, Rajidae): anatomy, behaviour and analogies to tetrapod locomotion. Biol. J. Linn. Soc. 77:35–41
McGhee GR Jr. 2001. The “multiple impacts hypothesis” for mass extinction: a comparison of the Late
Devonian and the late Eocene. Palaeogeogr. Palaeoclimat. Palaeoecol. 176:47–58
McGonnell I, Graham A. 2002. Trunk neural crest has skeletogenic potential. Curr. Biol. 12:767–71
Metscher BD, Takahashi K, Crow K, Amemiya C, Nonaka DF, Wagner GP. 2005. Expression of Hoxa-11
and Hoxa-13 in the pectoral fin of a basal ray-finned fish, Polyodon spathula: implications for the origin of
tetrapod limbs. Evol. Dev. 7:186–95
Milner AC. 1994. The aı̈stopod amphibian from the Viséan of East Kirkton, West Lothian, Scotland. Trans.
R. Soc. Edinb.: Earth Sci. 84:363–68
Milner AR. 1993. The Paleozoic relatives of lissamphibians. Herpetol. Monogr. 7:8–27
Milner AR, Sequeira SEK. 1994. The temnospondyl amphibians from the Viséan of East Kirkton, West
Lothian, Scotland. Trans. R. Soc. Edinb.: Earth Sci. 84:331–61
Milner AR, Smithson TR, Milner AC, Coates MI, Rolfe WDI. 1986. The search for early tetrapods. Mod.
Geol. 10:1–28
Panchen AL, Smithson TR. 1987. Character diagnosis, fossils, and the origin of tetrapods. Biol. Rev. 62:341–
438
Paton RL, Smithson TR, Clack JA. 1999. An amniote-like skeleton from the Early Carboniferous of Scotland.
Nature 398:508–13
Pridmore PA. 1995. Submerged walking in the epaulette shark Hemiscyllium ocellatum (Hemiscyllidae) and its
implications for locomotion in rhipidistian fishes and early tetrapods. Zool. Anal. Compl. Syst. 98:278–97
Rosen DE, Forey PL, Gardiner BG, Patterson C. 1981. Lungfishes, tetrapods, paleontology and plesiomorphy.
Bull. Am. Mus. Nat. Hist. 167:159–276
Ruta M, Bolt JR. 2006. A reassessment of the temnospondyl amphibian Perryella olsoni from the Lower Permian
of Oklahoma. Trans. R. Soc. Edinb.: Earth Sci. 97:113–65
Ruta M, Clack JA. 2006. A review of Silvanerpeton miripedes, a stem amniote from the Lower Carboniferous
of East Kirkton, West Lothian, Scotland. Trans. R. Soc. Edinb.: Earth Sci. 97:31–63
ANRV360-ES39-27
590
Coates
· ·
Ruta
Friedman
ANRV360-ES39-27
ARI
29 August 2008
21:3
Ruta M, Coates MI. 2007. Dates, nodes and character conflict: addressing the lissamphibian origin problem.
Ruta M, Coates MI, Quicke DLJ. 2003. Early tetrapod relationships revisited. Biol. Rev. 78:251–345
Ruta M, Wagner PJ, Coates MI. 2006. Evolutionary patterns in early tetrapods. I. Rapid initial diversification
followed by decrease in rates of character change. Proc. R. Soc. London Ser. B 273:2107–11
Ryan RJ, Boehner RC, Calder JH. 1991. Lithostratigraphic revisions of the Upper Carboniferous to Lower
Permian strata in the Cumberland Basin, Nova Scotia and the regional implications for the Maritimes
Basin in Atlantic Canada. Bull. Can. Petrol. Geol. 39:289–314
Säve-Söderbergh G. 1932. Preliminary note on Devonian stegocephalians from East Greenland. Medd.
Grönland 94:1–107
Schultze HP. 1991. A comparison of controversial hypotheses on the origin of tetrapods. See Schultze &
Trueb 1991, pp. 29–67
Schultze HP, Trueb L, eds. 1991. Origins of the Higher Groups of Tetrapods: Controversy and Consensus. Ithaca,
NY: Cornell Univ. Press
Scott AC, Glasspool IJ. 2006. The diversification of Paleozoic fire systems and fluctuations in atmospheric
oxygen concentrations. Proc. Natl. Acad. Sci. USA 103:10861–65
Shubin NH, Daeschler EB, Coates MI. 2004. The early evolution of the tretrapod humerus. Science 304:90–93
Shubin NH, Daeschler EB, Jenkins FA Jr. 2006. The pectoral fin of Tiktaalik roseae and the origin of the
tetrapod limb. Nature 440:764–71
Smithson TR. 1994. Eldeceeon rolfei, a new reptiliomorph from the Viséan of East Kirkton, West Lothian,
Smithson TR, Carroll RL, Panchen AL, Andrews SM. 1994. Westlothiana lizziae from the Viséan of East
Kirkton, West Lothian, Scotland, and the amniote stem. Trans. R. Soc. Edinb.: Earth Sci. 84:383–412
Streel M, Caputo MV, Loboziak S, Melo JHG. 2000. Late Frasnian-Famennian climates based on palynomorph analyses and the question of the Late Devonian glaciations. Earth Sci. Rev. 52:121–73
Tanaka M, Tickle C. 2007. The development of fins and limbs. In Fins into Limbs: Evolution, Development, and
Transformation, ed. BK Hall, pp. 65–78. Chicago: Univ. Chicago Press
Tarchini B, Duboule D. 2006. Control of hoxd genes’ collinearity during early limb development. Dev. Cell
10:93–103
Valentine JW. 1980. Determinants of diversity in higher taxonomic categories. Paleobiology 6:444–50
Vallin G, Laurin M. 2004. Cranial morphology and affinities of Microbrachis, and a reappraisal of the phylogeny
and lifestyle of the first amphibians. J. Vert. Paleontol. 24:56–72
Vorobyeva EI, Schultze HP. 1991. Description and systematics of panderichthyid fishes with comments on
their relationship to tetrapods. See Schultze & Trueb 1991, pp. 68–109
Wagner GP, Chiu CH. 2001. The tetrapod limb: a hypothesis on its origin. Mol. Dev. Evol. 291:226–40
Wagner PJ. 2001. Constraints on the evolution of form. In Palaeobiology II, ed. DEG Briggs, PR Crowther,
pp. 154–59. Oxford: Blackwell
Wagner PJ, Ruta M, Coates MI. 2006. Evolutionary patterns in early tetrapods. II. Differing constraints on
available character space among clades. Proc. R. Soc. London Ser. B 273:2113–18
Ward P, Labandeira C, Laurin M, Berner RA. 2006. Confirmation of Romer’s Gap as a low oxygen interval
constraining the timing of initial arthropod and vertebrate terrestrialization. Proc. Natl. Acad. Sci. USA
103:16818–22
Warren A. 2007. New data on Ossinodus pueri, a stem tetrapod from the Early Carboniferous of Australia.
J. Vert. Paleontol. 27:850–62
Watson DMS. 1920. The structure, evolution and origin of the Amphibia. The “Orders” Rachitomi and
Stereospondyli. Philos. Trans. R. Soc. London 209:1–73
Wellik DM, Capecchi MR. 2003. Hox10 and Hox11 genes are required to globally pattern the mammalian
skeleton. Science 301:363–67
Westoll TS. 1938. Ancestry of the tetrapods. Nature 141:127–28
Wilga CD, Lauder GV. 2001. Functional morphology of the pectoral fins in bamboo sharks, Chiloscyllium
plagiosum: benthic vs pelagic station-holding. J. Morphol. 249:195–209
Witten PE, Huysseune A. 2007. Mechanisms of chondrogenesis and osteogenesis in fins. In Fins into Limbs:
Evolution, Development, and Transformation, ed. BK Hall, pp. 79–92. Chicago: Univ. Chicago Press
591
ANRV360-ES39-27
ARI
29 August 2008
21:3
Zákány J, Fromental-Ramain C, Warot X, Duboule D. 1997. Regulation of number and size of digits by
posterior Hox genes: A dose-dependent mechanism with potential evolutionary implications. Proc. Natl.
Acad. Sci. USA 94:13695–13700
Zhu M, Ahlberg PE. 2004. The origin of the internal nostril of tetrapods. Nature 432:94–97
Zhu M, Ahlberg PE, Zhao W, Jia L. 2002. First Devonian tetrapod from Asia. Nature 420:760
592
Coates
· ·
Ruta
Friedman

Ever Since Owen: Changing Perspectives on the Early Evolution of

Transcription

Similar documents

PALEOZOIC ERA

DOWNLOAD 21 to Burn`s Press Kit Here

devonian spores from outer trøndelag, norway nor

full text

Importante

spiegle

Genesis: Paleozoica - The Origins Museum Institute